MINIREVIEW Those Amazing Dinoflagellate Chromosomes

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MINIREVIEW Those Amazing Dinoflagellate Chromosomes Cell Research (2003); 13(4):215-217 http://www.cell-research.com MINIREVIEW Those amazing dinoflagellate chromosomes PETER J RIZZO Department of Biology, Texas A & M University, College Station, TX 77843, USA E-mail: [email protected] ABSTRACT Dinoflagellates are a very large and diverse group of eukaryotic algae that play a major role in aquatic food webs of both fresh water and marine habitats. Moreover, the toxic members of this group pose a health threat in the form of red tides. Finally, dinoflagellates are of great evolutionary importance, because of their taxo- nomic position, and their unusual chromosome structure and composition. While the cytoplasm of dinoflagel- lates is typically eukaryotic, the nucleus is unique when compared to the nucleus of other eukaryotes. More specifically, while the chromosomes of all other eukaryotes contain histones, dinoflagellate chromosomes lack histones completely. There are no known exceptions to this observation: all dinoflagellates lack histones, and all other eukaryotes contain histones. Nevertheless, dinoflagellates remain a relatively unstudied group of eukaryotes. Key words: dinoflagellates, chromosomes, histones, histone-like proteins. INTRODUCTION above features are present in other protists, dinoflagel- lates are the only eukaryotes known to lack histones Dinoflagellate nuclei and chromosomes have been completely. This bizarre feature, found in all di- reviewed previously[1-3]. Although these reviews were noflagellate chromosomes, is so strange that it is often published some time ago, our understanding of the overlooked in textbooks and review articles[4]. ultrastructure and biochemistry of dinoflagellate chro- mosomes has not advanced significantly since these Uninucleate dinoflagellates reviews were published, and the dinoflagellate chro- mosome remains enigmatic[3]. Thus the purpose of Most dinoflagellates are uninucleate in that they this "minireview" is to stimulate interest in dinoflagel- contain one nucleus, as opposed to binucleate lates and their amazing chromosomes, rather than to dinoflagellates, which contain two. The latter have an attempt a comprehensive review of the more recent additional nucleus, present in an endosymbiont alga. literature on the structure and composition of the di- The nucleus of uninucleate dinoflagellates is usually noflagellate chromosome. termed "dinokaryotic", due mainly to the ultrastruc- While dinoflagellates constitute a very large and ture of the permanently condensed, "banded" chro- diverse group of algae, they all share some common mosomes[3]. This unique chromosome ultrastructure features in regard to the nucleus. To metion a few, is the same in all dinokaryotic nuclei, in both uninucle- dinoflagellates all have numerous, identically appear- ate and binucleate dinoflagellates, with very few ing chromosomes which remain condensed through- exceptions. out the cell cycle, and are bounded by a rather typical Another characteristic of dinokaryotic nuclei is that eukaryotic nuclear envelope, which remains intact they usually contain relatively large amounts of DNA throughout the cell cycle[1-3]. Although some of the [1-3]. Indeed, some DNA content estimates are ex- Those amazing dinoflagellate chromosomes http://www.cell-research.com tremely high, as in the case of Lingulodinium polyedrum ties that we call chromosomes? These are difficult evo- (formerly known as Gonyaulax polyedra). The DNA lutionary questions to answer, and there is no con- content for this dinoflagellate was reported to be 200 sensus as to which interpretation is correct. It is worth pg/cell, as determined by a fluorometric measurement noting however, that there is no connection between on whole cells using 3, 5-diaminobenzoic acid dinokaryotic chromosomes and metaphase dihydrochloride[5]. Apparently, fluorometric measure- chromosomes, polytene chromosomes, or the chroma- ments of DNA depend heavily on the fluorescent com- tin of the ciliate macronucleus. The dinokaryotic chro- pound used. For example, we obtained a value of 59 mosome is unique to dinoflagellates. pg/nucleus as determined in L. polyedrum whole cells using 4', 6-diamidino-2-phenylindole dihydrochloride Dinoflagellate histone-like proteins (HLPs) (DAPI), [Morris and Rizzo, unpublished data]. One Although the DNA of dinoflagellate chromosomes possible reason for the different values is that the par- lacks histones and nucleosomes, the chromosomes do ticular fluorescent compound used can give different contain a small amount of basic protein that has been results depending on the A/T and G/C content of the termed "histone-like"[1-3, 6-8]. These DNA-binding DNA being measured. proteins are within the molecular weight range of In any case, the presence of such large amounts of histones, and are basic by virtue of their high lysine DNA in a unicellular organism brings up questions as content. However, there is no homology between the to the function(s) of all this DNA. Clearly, most of this histone-like proteins in dinoflagellates, and those of DNA cannot code for proteins. The possibility exists prokaryotes (and cytoplasmic organelle DNA), as well that a large part of the DNA of dinoflagellate chromo- as any of the histones. These histone-like proteins are somes functions in a structural manner, but there is therefore unique to dinoflagellate chromosomes. The no evidence for, or against this speculation. Moreover, histone-like proteins in every uninucleate dinoflagel- it is difficult to imagine how RNA polymerase could late studied thus far, reveals one or two bands, as ex- gain access to the DNA in the "body" of the amined by gel electrophoresis. The putative function chromosome, since the chromosomes are permanently of these proteins is still unknown, but there is some condensed. Suggestions have been made that the main speculation that they may have a regulatory function body of the chromosome is not accessible to RNA in regard to transcription[7]. Some of these HLPs have polymerase, and only the DNA strands at the periph- been sequenced[7-9], and the HLPs from different ery of the chromosome are transcribed[2]. dinoflagellates are similar, but not identical to one The nuclear DNA of "typical" eukaryotes is com- another. posed of subunits called nucleosomes, which are formed when the DNA wraps around a "histone Binucleate dinoflagellates octamer" (two each of histones H2A, H2B, H3 and H4). These nucleosomes are connected by 60 base pair A few dinoflagellates are known to contain an stretches of DNA termed "linker DNA". A fifth his- endosymbiont alga which contributes a second nucleus tone (H1), "coils" these strands of nucleosomes into a [10-13]. These have been termed binucleate 30-nm fiber[3]. This represents the basic structure of dinoflagellates. It should be stressed that the endo- eukaryotic chromatin, which is further compacted by symbiont nucleus is within the confines of the endo- higher levels of folding by nonhistone proteins, and symbiont plasma membrane, and does not share a ultimately forms the metaphase chromosome. It is dif- common cytoplasm with the dinokaryotic nucleus. For ficult to imagine how dinoflagellates achieved the for- lack of a better term, the endosymbiont nucleus is mation of morphologically distinct chromosomes in the usually called the "eukaryotic" nucleus, to differenti- absence of histones, when all other eukaryotes con- ate it from the host (dinokaryotic) nucleus. Oddly tain histones and resulting nucleosomes. Did di- enough, the endosymbiont nucleus contains histones, noflagellates originally contain histones and nucleo- but not morphologically distinct chromosomes[13]. To somes and somehow lost them? Or did they never con- retain the endosymbiont condition, nuclear and cell tain histones, and somehow found an alternative way division in the host and endosymbiont must be to condense large amounts of DNA into discrete enti- synchronized. Cell division is triggered by division of 216 Cell Research 13(4), Aug, 2003 Peter J RIZZO the dinokaryotic nucleus (Dr. Elenor Cox, personal major histone-like protein, HGm. J Phycol 2000; 36:584-9. communication). Subsequently, the endosymbiont 7. Chudnovsky Y, Li JF, Rizzo PJ, Hastings JW, Fagan TF. Cloning, expression, and charactertization of a histone-like nucleus pinches in two. protein from the marine dinoflagellate Lingulodinium Recently, there has been an increase of dinoflagel- polyedrum (Dinophyceae). J Phycol 2002; 38:1-9. late "blooms", or red tides. One such bloom was caused 8. Sala-Rovira M, Geraud ML, Caput D, Jacques F, Soyer- by the binucleate dinoflagellate Kryptoperidinium Gobillard M-O, Vernet G, Herzog M. Molecular cloning and foliaceum (formerly known as Peridinium foliaceum immunolocalization of two variants of the major basic nuclear protein (HCc) from the histone-less eukaryote [14]. Interestingly, on further examination, the bloom Crypthecodinium cohnii (Pyrrhophyta). Chromosoma 1991; isolate was shown to lack the endosymbiont nucleus, 100:510-8. suggesting a transient endosymbiont association[14]. 9. Taroncher-Oldenburg G, Anderson DM. Identification and Although binucleate dinoflagellates are very characterization of three differentially expressed genes en- coding S-adenosylhomocysteine hydrolase, methionine interesting, and also understudied, the focus of this aminopeptidase and a histone-like protein in the toxic di- review is on the dinokaryotic chromosome. Therefore noflagellate Alexandrium fundyense. Appl Environ Microbiol the acquisition and maintenance of the binucleate con- 2000; 66:2105-12.
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